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Can Root-Associated Fungi Mediate the Impact of Abiotic Conditions on the Growth of a High Arctic Herb?

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Can Root-Associated Fungi Mediate the Impact of Abiotic Conditions on the Growth of a High Arctic Herb? bioRxiv preprint doi: https://doi.org/10.1101/2020.06.20.157099; this version posted June 20, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. Can root-associated fungi mediate the impact of abiotic conditions on the growth of a High Arctic herb? 1,2* 2 1,3,4 1 Magdalena Wutkowska ,​ Dorothee Ehrich ,​ Sunil Mundra ,​ Anna​ Vader ,​ Pernille ​ ​ ​ ​ ​ ​ ​ B. Eidesen1 ​ 1 ​ Department of Arctic Biology, The University Centre in Svalbard, Longyearbyen, Norway 2 ​ Department of Arctic and Marine Biology, UiT – The Arctic University of Norway, Tromsø, Norway 3 ​ Department of Biosciences, University of Oslo, Oslo, Norway 4 Department of Biology, College of Science, United Arab Emirates University, Abu Dhabi, United Arab Emirates *corresponding author: [email protected] ABSTRACT Arctic plants are affected by many stressors. Root-associated fungi are thought to influence plant performance in stressful environmental conditions. However, the relationships are not transparent; do the number of fungal partners, their ecological functions and community composition mediate the impact of environmental conditions and/or influence host plant performance? To address these questions, we used a common arctic plant as a model system: Bistorta vivipara. Whole plants (including root system) were collected from nine ​ ​ locations in Spitsbergen (n=214). Morphometric features were measured as a proxy for performance and combined with metabarcoding datasets of their root-associated fungi (amplicon sequence variants, ASVs), edaphic and meteorological variables. Seven biological hypotheses regarding fungal influence on plant measures were tested using structural equation modelling. The best-fitting model revealed that local temperature affected plants both directly (negatively aboveground and positively below-ground) and indirectly - mediated by fungal richness and the ratio of symbio- and saprotrophic ASVs. Fungal community composition did not impact plant measurements and plant reproductive investment did not depend on any fungal parameters. The lack of impact of fungal community composition on plant performance suggests that the functional importance of fungi is more important than their identity. The influence of temperature on host plants is therefore complex and should be examined further. KEY WORDS plant-microbe interaction, plant performance, root-associated fungi, arctic soil biology, below-ground vegetation 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.06.20.157099; this version posted June 20, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. Introduction Arctic plants are facing many environmental constraints for growth, such as short vegetation season, consistent cold, limitation of nutrients or cyclic physical disturbances, i.e. 1 cryoturbation .​ These plants have evolved a range of adaptations to cope with the prevailing ​ 2–4 conditions, including being perennial and allocating most of their biomass below-ground .​ ​ Being perennial provides a resource-saving advantage in nutrient-poor habitats with low temperatures that slow down biochemical reactions and therefore also growth, whereas the benefits of biomass allocation to below ground parts include increased area of nutrient absorption. Because of nutrient scarcity, the interface between plant and soil is of relatively 3 greater importance in the Arctic than in other biomes .​ A significant part of the soil-plant ​ interface is inhabited by microbes, including roots-associated fungi (RAF). Arctic RAF 5–7 consist mostly of symbiotrophic fungi, especially ectomycorrhizal fungi .​ These fungi ​ efficiently increase the volume of soil that can be penetrated in search for resources, such as 8 nutrients from seasonally or newly thawed permafrost .​ The most severe limitations for ​ 1,9 growth observed in arctic plants are due to low temperatures and resource limitation ,​ ​ suggesting that the relationship with RAF might play a crucial role in plant survival and growth. Multiple characteristics of species communities play an essential role in the functioning of 10–13 ecosystems, such as richness, abundance or community structure .​ Based on previous ​ findings, we may expect that the more diverse the community of RAF, the better for a host 14 plant .​ However, it is not clear how these characteristics of RAF communities impact their ​ host plants, especially in cold biomes. Symbiotic fungi provide resources and probably additional benefits mitigating possibly harmful effects of environmental stressors enhancing 15 plant growth and productivity .​ However, releasing root exudates of primary metabolites that ​ 16,17 can be absorbed by members of its microbiome does come with a cost for a plant .​ In ​ nitrogen-limited tundra in Alaska, 61-88% of plant nitrogen (N) was supplied from mycorrhizal fungi. In exchange, the plants delivered 8-17% of carbon (C) produced 18 photosynthetically to the fungi .​ A plant could perhaps increase the amount of released ​ nutritious root exudates to attract more species of symbiotrophic fungi that in turn, could potentially increase the amount of nitrogen delivered. However, higher fungal richness would increase competition for limited space in the rhizosphere and possibly for resources, although the mechanism is not yet fully described. Therefore, plants ‘living on the edge’ in the High Arctic may benefit from the selective choice of their members of RAF communities, 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.06.20.157099; this version posted June 20, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 19 favouring the most beneficial fungal partners for plant growth or mediation of stressors .​ In ​ this scenario, species richness in RAF communities would be irrelevant for plant performance. The presence of specific functional traits rather than their identity could be 20 more important .​ The vast array of interconnected biotic and abiotic factors occurring in ​ natural systems complicate uncovering if and how plants show preference among their 21 root-associated fungi among the pool of species present in the soil .​ ​ One approach to disentangle these often confounded factors are controlled experiments. Most of the experiments assessing the impact of RAF diversity on host plant performance 22 have focused on arbuscular mycorrhiza in crops ;​ whereas similar studies on ​ ectomycorrhizal (EcM) plant species come mostly from the pre-high throughput sequencing 14 era and have focussed on trees (e.g. ).​ Several experiments under controlled settings have ​ shown that EcM host plants may clearly benefit from their increased fungal richness, however, the tested level of richness was often incomparable with natural environments, 14 such as an increase from 1 to 4 species of EcM fungi .​ Some studies, however, did not find ​ any enhancements in plant performance mediated by EcM fungi or concluded that the 23 outcome of EcM species richness on plant productivity is context dependent .​ RAF diversity ​ was shown to be particularly sensitive to experimental conditions compared to fungi that 24 inhabit space further from the roots in the rhizosphere or bulk soil .​ Moreover, morphology ​ and physiology of lab-grown plants differ from those in the natural systems, e.g. by 25 increasing growth rate and higher concentrations of nutrients in tissues .​ All these ​ differences could affect and alter plant-associated organisms, such as RAF. Experimental procedures cannot consider all the complexity of natural systems and their effects do not always reflect those observed in the wild. Thus, observational studies can provide crucial complementary knowledge, in particular for extreme environments like the high Arctic. Species response to environmental shifts, including ongoing climate changes, is one of the crucial questions in natural sciences. It is a particularly outstanding issue in the Arctic where rates of temperature and precipitation are changing at the fastest pace in the world, and are 26,27 predicted to continue rising rapidly .​ These changes impact mechanisms that alter ​ biogeochemical cycles and determine critical ecosystem-climate feedback processes, such as the release of organic carbon of which nearly half of the global stock is stored in the Arctic 28,29 soils ​ ​ or increased growth of vascular plants. Such ecosystem feedbacks, which are ​ essential bricks in the understanding of global change, depend on complex relationships 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.06.20.157099; this version posted June 20, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 30 between abiotic and biotic factors in arctic soils .​ However, the biology of these soils ​ remains at present an understudied ‘black box’. To shed some light onto these soil processes, we used a plant-centric
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